Ammonia Oxidation in the Ocean Can Be Inhibited by Nanomolar Concentrations of Hydrogen Peroxide

Abstract

Marine Thaumarchaeota were discovered over 20 years ago and although a few isolates from this group are now available for study, we do not yet understand the environmental controls on their growth and distribution. Thaumarchaeotes oxidize ammonia to nitrite, mediating a key step in the global nitrogen cycle, and it is estimated that about 20% of all prokaryotic cells in the ocean belong to this phylum. Despite their almost ubiquitous distribution, marine Thaumarchaeota are rarely abundant in open-ocean surface (<100 m) waters. We tested the hypothesis that this vertical distribution is driven by reactive oxygen species (ROS), specifically H 2 O 2 , generated by photochemical and biological processes-"indirect photoinhibition" rather than light inhibition as previously postulated for ammonia-oxidizing Archaea. Here we show that H 2 O 2 can be surprisingly toxic to Thaumarchaeota from the Southern Ocean, with ammonia oxidation inhibited by additions of as little as 10 nM H 2 O 2 , while temperate Thaumarchaeota ecotypes were more tolerant. This sensitivity could explain the seasonal disappearance of Thaumarchaeota from polar surface waters and the increase in ammonia oxidation rates with depth commonly observed in marine environments. Our results highlight the need for further physiological studies of Thaumarchaeota, and indicate that ROS sensitivity could be used as a characteristic for dividing the group into meaningful ecotypes.

Changes in Marine Prokaryote Composition with Season and Depth Over an Arctic Polar Year

“…More recently, the cyclical rise (during winter) and decline (in summer) of the group in the surface waters of polar regions has received some attention (Murray et al, 1998(Murray et al, , 1999Church et al, 2003;Alonso-Sáez et al, 2008Grzymski et al, 2012;Williams et al, 2012) and indeed, our data confirmed these findings. The almost total disappearance of the Thaumarchaeota from the photic zone during the summer months ( Figure 5) is therefore suggestive of photoinhibition of ammonia oxidation (Guerrero and Jones, 1996;Murray et al, 1998;Mincer et al, 2007;Schleper and Nicol, 2010;Merbt et al, 2012), or has been more recently posited, a sensitivity to reactive oxygen species produced as a result of photosynthesis (Tolar et al, 2016). The reasons may however be multifactorial and it is thought that the Archaea may also be outcompeted by phytoplankton (Murray et al, 1998;Ward, 2000Ward, , 2005Church et al, 2003;Herfort et al, 2007;Smith et al, 2014) and Bacteria (which are much more active in the uptake of the labile bloomproduced substrates Alonso-Sáez et al, 2008;Kalanetra et al, 2009), or even subjected to selective viral infection (Labonté et al, 2015).…”

Relative impacts of light, temperature, and reactive oxygen on thaumarchaeal ammonia oxidation in the North Pacific Ocean

“…Hydrogen peroxide addition of 50 nmol L −1 did not have a negative effect on ammonia oxidation rates in any of the samples we studied, suggesting that it is not an important factor within our study area (Supporting Information Table S2). To critically evaluate this conclusion, we also compare our data for H 2 O 2 distribution with estimates of peroxide inhibition based on results from Tolar et al (). In that study, H 2 O 2 concentrations as little as 10 nmol L −1 were toxic to Thaumarchaea from the Southern Ocean (Tolar et al ).…”

“…For each analysis, we added 50 nmol L −1 15 and 50 nmol L −1 H 2 O 2 for the peroxide treatment ( n = 3) and only 15 to the control group ( n = 3). This concentration was selected as representative of H 2 O 2 at the base of the mixed layer throughout much of the cruise, so it represented a realistic intermediate value, and is comparable to the range of 10–300 nmol L −1 used by Tolar et al (). Following addition, the bottles were gently inverted to ensure that the hydrogen peroxide solution and 15 were evenly distributed and incubated for 24–25 h in the dark at in situ temperatures in a temperature‐controlled room.…”

“…Photoinhibition may also arise indirectly if photochemically produced species, such as hydrogen peroxide (H 2 O 2 ), adversely affect the physiology of AOA. Tolar et al () demonstrated that H 2 O 2 negatively affected ammonia oxidation rates in the ocean, and the effect appeared to be region and taxa specific. However, although the genome of Nitrosopumilis maritimus reveals no peroxidase or catalase genes (Walker et al ), it is not inhibited by relatively high concentrations of hydrogen peroxide (Qin et al ).…”

Cross‐protection from hydrogen peroxide by helper microbes: the impacts on the cyanobacterium Prochlorococcus and other beneficiaries in marine communities

“…Tolar et al discovered that the oxidation of ammonia by marine AOA's could be inhibited by amendments as small as 10 nM HOOH (Tolar et al, 2016). Tolar et al discovered that the oxidation of ammonia by marine AOA's could be inhibited by amendments as small as 10 nM HOOH (Tolar et al, 2016).…”